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Contents lists available at ScienceDirect

Journal for Nature Conservation

journal homepage: www.elsevier.de/jnc

The role of native forest plantations in the conservation of Neotropical

birds: the case of the Andean alder
a,b,c

Gabriel J. Castano-Villa
, Jaime V. Estevez a,b,d , Francisco E. Fontrbel c,
a

Departamento de Desarrollo Rural y Recursos Naturales, Facultad de Ciencias Agropecuarias, Universidad de Caldas, Colombia
Grupo de Investigacin en Ecosistemas Tropicales, Universidad de Caldas, Colombia
Departamento de Ciencias Ecolgicas, Facultad de Ciencias, Universidad de Chile, Chile
d
Departamento de Biologa, Facultad de Ciencias Exactas y Naturales, Universidad de Caldas, Colombia
b
c

a r t i c l e

i n f o

Article history:
Received 11 January 2014
Received in revised form 8 August 2014
Accepted 19 August 2014
Keywords:
Alnus acuminata
Bird conservation
Colombia
Community similarity
Species richness
Threatened species

a b s t r a c t
The gradual increase in reforested areas worldwide, as a strategy for mitigating native forest loss, has
stressed the need of assessing their real value as habitat for native species. Forest plantations, particularly those based on native species, could be valuable for conservation purposes, especially in heavily
fragmented and disturbed ecosystems. We evaluated the value of a monoculture of a native tree species,
the Andean alder (Alnus acuminata), for the conservation of avifauna in the Central Andes region, which is
considered a bird species diversity hotspot but also suffers from high anthropogenic disturbance levels.
Our results suggest that alder plantations are valuable for conservation from three points of view: (1)
they have similar or greater bird species richness and abundance than secondary native forests; (2) low
community similarities are found between this type of forest compared to secondary forest stands (with
27 species exclusive to alder plantations); and (3) three near threatened species (Odontophorus hyperythrus, Eriocnemis derbyi, and Cyanolyca viridicyanus). Further, 27 out of the 85 species found at the alder
plantations were of least concern but showing decreasing population trends. While forest plantations do
not replace native forests, they offer habitat for many bird species, some of them being of conservation
concern (i.e., included in an IUCN threat category) or with decreasing populations. Hence establishing
native species plantations among native forest remnants especially in heavily fragmented landscapes
could have a positive effect in the conservation of threatened avifauna.
2014 Elsevier GmbH. All rights reserved.

Introduction
Many agroecosystems may constitute a habitat for native
species in anthropogenic-altered landscapes. This is particularly
relevant because of increasing anthropogenic disturbances, reduction of native forest cover, and gradual biodiversity losses (Barlow
et al., 2007; Holbech, 2009; Peh et al., 2006), which lead many bird
populations to decrease. Few studies have evaluated the potential role of native forest plantations as habitat for threatened bird
species (Faria et al., 2007; Farwig et al., 2009; Proenca et al.,
2010). Those studies have provided valuable information about
the potential value and limitations of forest plantations for species
conservation.

Corresponding author at: Facultad de Ciencias, Universidad de Chile, Las

noa

Palmeras 3425, Nu
7800024, Santiago, Chile. Tel.: +56 2 29787438;
fax: +56 2 22727363.
E-mail address: fonturbel@gmail.com (F.E. Fontrbel).

One of the main limitations of the potential species conservation value of forest plantations is that these forest types are usually
associated with species with low forest dependency or habitat generalists, which are not of conservation concern. Thus many of the
species commonly found in those habitats are usually less sensitive to habitat disturbance, and very few are of worldwide or local
conservation concern (Farwig et al., 2009; Petit & Petit, 2003; Sodhi
et al., 2005). This appears to be limiting the conservation potential
of forest plantations, as extinction-prone species are usually forest
specialists (Renjifo, 1999; Ribon et al., 2003).
Within the Neotropics, the Colombian Central Andes region is
considered a conservation priority worldwide due to its high proportion of endemic bird species (Statterseld et al., 1998), loss and
fragmentation of its natural forests (Birdlife International, 2012),
and their associated local extinctions (Renjifo, 1999). In this region,
many monospecic forest plantations of native species have been
planted since 1970 in order to protect soils and watersheds, the
Andean alder (Alnus acuminata, Betulaceae) being a well-known
example (Murcia, 1997).

http://dx.doi.org/10.1016/j.jnc.2014.08.010
1617-1381/ 2014 Elsevier GmbH. All rights reserved.

Please cite this article in press as: Castano-Villa,

G. J., et al. The role of native forest plantations in the conservation of Neotropical birds:
the case of the Andean alder. Journal for Nature Conservation (2014), http://dx.doi.org/10.1016/j.jnc.2014.08.010

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The actual value of Andean alder reforestation on species-level

biodiversity in the Andes remains little explored. However, Murcia
(1997) stated that these plantations may contribute to the natural regeneration of the native forest. Alnus acuminata has a catalyst
effect on forest regeneration, as this fast-growing tree allows other
species to recruit and also improves soil through nitrogen xation.
Further, Kattan and Murcia (2012) stated that alder plantations
are structurally similar to secondary native forest stands in some
aspects (basal area, stem density, and fallen logs). Considering that
habitat structure is a key factor for understanding bird species richness in tropical forests (Terborgh, 1985), alder plantations may
represent a conservation opportunity for avifauna.
To establish the real conservation value of mature (more than 40
years old, the oldest ones in the region) Andean alder plantations for
Neotropical threatened avifauna, we compared bird species richness and abundance in two forest types: Andean alder stands and
secondary forests of about the same age. Considering that A. acuminata is a native species, it shares an evolutionary history with the
native fauna, and the similar structure of alder plantations to a secondary forests of the same age (see Table 1 in Kattan & Murcia,
2012), we hypothesized that similar bird assemblages would be
found in the two forest types.

Materials and methods

Study area
The Central Hidroelctrica de Caldas S.A. E.S.P. (CHEC) Protective
Forest Reserve is owned and operated by the public hydropower
company (CHEC). The Reserve is located on the western slope of
the Colombian Central Andes (N 05 01 W 75 24 ; mean altitude
2500 m asl), and it is part of the basin of the Chinchin River, in
the region of Caldas. This zone has an average annual temperature of 13 C and an annual precipitation of 2500 mm. The Reserve
comprises 3890 ha covered with native forest stands in diverse successional stages (nonetheless, there are no accessible old-growth
stands in the study area), and several exotic (Eucalyptus spp., Acacia
spp., Pinus patula, and Cupressus lusitanica) and native (A. acuminata) plantations. Before 1970, most of this area was dominated by
agricultural activities, particularly pastures for cattle ranching, but
during the 1970s many areas were reforested and protected under
the initiative of CHEC.
We selected stands of about the same age (3540 years old,
based on information provided by the local communities) to avoid
confounding effects related to forest maturity and habitat structure,
which are associated with the resident avian community (Styring
et al., 2011). We chose four stands of alder plantation ranging
between 6 and 7 ha (26 ha in total), and four patches of secondary
native forest (mainly dominated by Montanoa quadrangularis
Asteraceae, Saurauia cuatrecasana Actinidiaceae, Lippia schlimii
Verbenaceae) ranging between 5 and 9 ha (30 ha in total). In
both cases, sampling locations were separated from each other by
a distance between 500 m and 1 km. These locations are currently
immersed in a landscape matrix with a heterogeneous mosaic of
exotic tree species plantations and native forests varying in age
and degree of disturbance, therefore reducing potential landscape
matrix effects. Ramos (2010) found no differences in basal area or
canopy height between these forest types, but understory height
was higher at the secondary forest. The alder plantation and secondary forest understories are similarly dense, reaching an average
height of 3 m. Common tree and shrub species found in the plantation included Bocconia frutescens (Papaveraceae), Miconia theaezans
(Melastomataceae), Palicourea acetosoides (Rubiaceae), Palicourea
calophlebia (Rubiaceae), and Sapium stylare (Euphorbiaceae). The
most common species found in the understory of the secondary

forest remnant were Palicourea deviae (Rubiaceae), Hoffmannia

glabra (Rubiaceae), Chamaedorea linearis (Arecaceae), Siparuna
laurifolia (Siparunaceae), and Piper spp. (Ramos, 2010). Plant
nomenclature followed the International Plant Names Index
(www.ipni.org).
Data collection and bird categorization
The avifauna present in each forest type (native secondary forest and alder plantation) was assessed using two complementary
methods: mist-netting and point counts. Both methods have been
used in similar studies in the tropics, due to their complementarity for accurately describing bird communities (Barlow et al.,
2007; Holbech, 2009). Between October 2008 and April 2009 we
established two mist-net capture points in each stand and patch
(i.e., eight for each forest type) separated 100 m from each other,
which were operated on a monthly basis. We set four mist-nets
(12 2.5 m 36 mm) at each capture point for 56 h per month, with
a total capturing effort of 3136 h net1 . Captured birds were marked
using bands with a unique color combination for individualization
and then released. To ensure independence of the observations
among capture points, we did not include recaptures in the analyses. For the point counts we estimated the total number of birds
detected within a xed-radius of 20 m (Hutto et al., 1986). This
detection distance was chosen following a previous eld study in
which we determined that 20 m allowed for detection of most of the
species present at the secondary forests and the alder plantations,
with similar detection probabilities. Point counts were performed
at the same locations as mist-netting, at least 100 m apart from
each other. At each point count, we registered all observed and
heard bird species for 20 min (total counting effort = 1120 min per
forest type). Each counting was made between 6:00 and 10:00 h,
and between 14:00 and 18:00 h. We did not count birds on rainy
or misty days. To avoid temporal autocorrelation among observations (i.e., counting the same bird in neighboring point counts) we
censused neighboring stands or patches on different days. Also, to
minimize recounting we individualized birds detected at the counting points using the colored bands that we set when mist-nets
were operated. Family classication of bird species was performed
following Remsen et al. (2014). Species were considered as threatened when they were included in any of the International Union
for Conservation of Nature categories (near threatened, vulnerable
or endangered; IUCN, 2012).
Bird species were categorized using two criteria: (1) population
trend (increasing, stable, or decreasing) according to IUCN (2012);
and (2) sensitivity to disturbance (high, medium, or low) according
to Stotz et al. (1996); species with high sensitivity to disturbance
are known to be the most affected by anthropogenic habitat modications.
Data analysis
Comparisons of the mean number of bird species present
between native forest and alder plantation sites were made through
visual inspection of the 95% condence interval overlapping of the
rarefaction curves based on abundances (Barlow et al., 2007). This
technique standardizes sample comparisons based on the number
of individuals, allowing comparison of species richness at the same
level of abundance (Gotelli & Colwell, 2001). Rarefaction curves
were constructed using Ecosim 7, and employing 1000 iterations in
each case (Gotelli & Entsminger, 2007). An estimate of the expected
species richness in each forest type was calculated with EstimateS
8.2 (Colwell, 2009), utilizing the mean of four commonly used
abundance-based estimators (ACE, Chao1, Jack1, and Bootstrap) as
described by Barlow et al. (2007). We considered each capture and
counting point as a sample unit (56 per forest type).

Please cite this article in press as: Castano-Villa,

G. J., et al. The role of native forest plantations in the conservation of Neotropical birds:
the case of the Andean alder. Journal for Nature Conservation (2014), http://dx.doi.org/10.1016/j.jnc.2014.08.010

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To compare bird community composition (in terms of species

abundance) between the alder plantation and the secondary forest, we performed a nested analysis of similarity (ANOSIM), which
is a permutational non-parametric test (Clarke, 1993). This analysis
was conducted using the BrayCurtis distance, a measure previously used for comparing bird communities (Barlow et al., 2007),
ANOSIM tests were performed with PAST 2.15 (Hammer et al.,
2001).
All abundance references (for mist-netting and point counts)
refer to indices of abundance derived from our sampling rather than
the real abundance, which is not known. Species richness and abundance comparisons were made among stands and patches (n = 4
for each forest type). Goodness-of-t to a normal distribution was
assessed through a ShapiroWilk test. Homogeneity of variances
was assessed using a Levene test. Richness and abundance were
compared using a one-way nested Analysis of Variance (ANOVA),
with point counts or mist-nettings point number nested within
forest type (Murcia, 1997). These analyses were performed using
STATISTICA 7 (StatSoft, 2004). We reported only those results that
were statistically signicant (at an = 0.05 condence level).

Results
We recorded a total of 103 bird species (Table S1, available in
Online Supplementary Material), 85 in the alder plantations and 76
in the secondary forest stands. Mean species richness, determined
by the rarefaction method, showed signicantly greater values in
alder plantations than in secondary forest stands using mist-netting
data (Fig. 1A), and comparing the curves at the same number of captures (222). However, species richness between plantations and
secondary forest stands was similar using the point count data
(Fig. 1B), as the 95% condence intervals of the rarefaction curves
overlapped at the same number of records (429). Rarefaction curves
obtained from point counts reached an asymptote, whereas those
obtained from mist-netting did not reach an asymptotic value.
This indicates that the sampling effort obtained by point counts
was enough for a proper recording of bird species in each forest
type, while mist-netting data should be interpreted with caution.
According to the richness estimators calculated, alder plantations
have 7097 species (considering both sampling methods), while
secondary forest stands have an expected richness of 6566 species
(Table 1). Overall abundance was signicantly greater in alder plantations compared to secondary forest stands (51.7 6.1 individuals
at the plantation and 29.3 2.8 at the native forest; F1,6 = 44.83,
p < 0.001) using capture data, but abundances were similar in point
counts (80.2 2.9 individuals at the plantation and 65.6 16.2 at
the native forest; F1,6 = 3.15, p = 0.126).
When analyzing species richness according to their population
trends and sensitivity to habitat disturbance categories, alder plantations had signicantly greater species richness for those species
with a decreasing population trend (13.5 1.5 species at the plantation and 10.1 1.9 at the native forest; F1,6 = 6.77, p = 0.040 for
point count data) as well as for species with a stable population
trend (11.0 3.0 at the plantation and 6.9 0.6 at the native forest; F1,6 = 7.12, p = 0.037 for mist-netting data); species with an
increasing population trend were similar between plantations and
secondary forest stands. Conversely, species with medium disturbance sensitivity had signicantly greater species richness in
alder plantations (15.7 2.1 at the plantation and 11.1 2.1 at the
native forest; F1,6 = 9.89, p = 0.020 for mist-netting data), while the
richness of those species with high sensitivity to habitat disturbance (the most affected by anthropogenic disturbance) was similar
between plantations and secondary forests (i.e., differences were
not signicantly different for both mist-nets and point counts). A
similar trend was observed for species abundance. Those species

Fig. 1. Rarefaction curves showing mean species richness with 95% condence intervals for (A) mist-netting data and (B) point count data.

with decreasing (23.9 2.0 at the plantation and 15.6 3.6 at the
native forest, F1,6 = 16.38, p = 0.007 based on mist-netting data) and
stable (21.0 4.7 at the plantation and 9.4 1.9 at the native forest,
F1,6 = 21.15, p = 0.004 based on mist-netting data) population trends
were signicantly more abundant in alder plantations, whereas
the abundance of species showing an increasing trend was similar between plantations and secondary forest stands. Species with
medium sensitivity to disturbance were signicantly more abundant in alder plantations (36.4 3.9 at the plantation and 19.9 2.7
at the native forest; F1,6 = 48.85, p < 0.001 based on mist-netting
data), while the abundance of species with low and high sensitivity to disturbance was similar between native forest and alder
plantation sites.
Avifauna composition between plantations and secondary forest stands was signicantly different with both mist-netting
(ANOSIM, R = 0.36, p < 0.001) and point count (R = 0.63, p < 0.001)
data. Of the 85 species recorded in alder plantations, 27 were
exclusive to this forest type, while 18 of 76 species were exclusive to secondary forest stands. Of those 18 species only found in
secondary forest stands, three species are considered of conservation concern according to IUCN: two categorized as vulnerable
(Leptosittaca branickii, and Hapalopsittaca amazonina); and one as
endangered (Scytalopus canus) by IUCN. On the other hand, two
near threatened species (Odontophorus hyperythrus and Eriocnemis derbyi) were found exclusively in the plantations, and the
near threatened species Cyanolyca viridicyanus was found in both

Please cite this article in press as: Castano-Villa,

G. J., et al. The role of native forest plantations in the conservation of Neotropical birds:
the case of the Andean alder. Journal for Nature Conservation (2014), http://dx.doi.org/10.1016/j.jnc.2014.08.010

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Table 1
Observed and expected species richness for alder plantations and secondary forest stands estimated from mist-netting (MN) and point counts (PC). The expected species
richness was calculated by the mean value of the ACE, Chao1, Jack1, and Bootstrap estimators.
Forest type

Andean alder plantation

Andean alder plantation
Secondary forest
Secondary forest

Method

MN
PC
MN
PC

Number of records

414
642
234
525

forest types. Additionally, 32% of the species categorized as least

concern at the alder plantation also show decreasing population
trends, six of them (O. hyperythrus, E. derbyi, Poecilotriccus ruceps,
Cinnycerthia unirufa, Conirostrum albifrons, and Catamblyrhynchus
diadema) were found exclusively at these plantations.
Discussion
The value of forest plantations for avifauna conservation has
been evaluated from three points of view: (1) species richness
and abundance; (2) community similarity; and (3) the conservation status and population trends of species (Barlow et al., 2007;
Greenberg et al., 2000; Petit & Petit, 2003; Rotenberg, 2007). Those
points of view are not mutually exclusive but complementary, and
they allow a less biased evaluation of the actual conservation value
of plantations. In this study, we evaluated those three points of
view independently, and all of them showed that alder plantations appear to contribute to bird conservation. Both observed and
expected species richness in alder plantations were equal to or
greater than those recorded in secondary forests. These results
are consistent with those reported by other studies regarding
monospecic plantations with native species in tropical (Farwig
et al., 2009), subtropical (Volpato et al., 2010), and temperate
regions (Proenca et al., 2010).
Contrary to our hypothesis, the similarity between bird communities in alder plantations and secondary forest stands was low. This
result may be related to differences in habitat structure (Terborgh,
1985) between native forests and plantation stands, given in this
particular case to understory height and vegetation density (Ramos,
2010). We found greater richness and abundance of species with
medium sensitivity to habitat disturbance and decreasing populations in alder plantations compared to secondary forest stands.
These two characteristics are determinant factors of bird vulnerability in the tropics, and stress the value of alder plantations in terms
of conservation (Petit & Petit, 2003). Furthermore, some of the
declining species present in these plantations are highly specialized
(following Loiselle & Blake, 1992) to forest habitats (e.g., Dendrocincla tyrannina, Dendrocolaptes picumnus, Xiphorhynchus triangularis,
Cinnycerthia olivascens, and Hemispingus atropileus), and because
of those traits they were recorded as locally extinct from forest

fragments and other regions of the Central Andes (Castano-Villa

2008; Renjifo, 1999). It is also remarkable that a

& Patino-Zabala,
considerable amount of the species found in alder plantations are
of least concern but showing decreasing population trends (27 out
of 85 species). The fact that these species might be threatened in
the future stresses the role of native plantations among secondary
forest remnants.
Six threatened species were found in our study area, two of them
(O. hyperythrus and E. derbyi) exclusively in alder plantations. These
species were classied as near threatened, and are currently jeopardized by habitat loss. On the contrary, the conspicuous absence
of two vulnerable species (L. branickii and H. amazonina, Psittasidae) in plantations is perhaps explained because they are canopy
frugivores and are unable to nd palatable fruits among plantation
trees. This result may reect a limited value of alder plantations

Species richness

Sampling effectiveness

Observed

Expected

71
62
49
60

97
70
66
65

73%
89%
74%
92%

to conserve canopy-foraging frugivorous birds. However, we registered a total of 30 frugivorous bird species (mainly those belonging
to the families Ramphastidae, Turdidae, Thraupidae, and Emberizidae) at the alder plantations, which might be contributing to the
regeneration of the natural vegetation.
While we do not consider alder plantations as a surrogate for
secondary forests, in this case setting them among native forest
remnants could be valuable for bird conservation by contributing to
species richness, complementing other forest types, and harboring
threatened and potentially threatened species that are currently
showing decreasing population trends. Given the high anthropic
disturbance levels characterizing the Central Andes region, where
most of the natural forests have been impacted and the few
old-growth remaining stands are scattered in inaccessible areas,
establishing plantations with native species among second-growth
native forest remnants may help to mitigate the effects of habitat
loss and fragmentation, which are the most threatening factors for
the avifauna in this region.

Acknowledgements
The authors are grateful to the Vicerrectora de Investigaciones
y Posgrados of the Universidad de Caldas (Grant no. 000414) and
to Fundacin HTM for providing funding. We are indebted to the
Central Hidroelctrica de Caldas S.A E.S.P. and to C.A. Franco for
arranging the logistics at the study site. L. Salazar, R. Santisteban,
A. Hoyos, A.D. Pineda, and F. Ramos assisted in the eld. The Corporacin Autnoma Regional de Caldas (CORPOCALDAS) granted
J.A. Simonetti, J.L. Tella,
the research permits. Comments of A. Vina,
and two anonymous reviewers helped to improve an earlier version of the manuscript. We appreciate the English correction made
by L. Eaton. GJCV and FEF were supported by CONICYT doctoral
fellowships.

Appendix A. Supplementary data

Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.jnc.2014.08.010.

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Please cite this article in press as: Castano-Villa,

G. J., et al. The role of native forest plantations in the conservation of Neotropical birds:
the case of the Andean alder. Journal for Nature Conservation (2014), http://dx.doi.org/10.1016/j.jnc.2014.08.010